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Protonation and Chloroplast Membrane Structure

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Protonation and Chloroplast Membrane Structure PROTONATION AND CHLOROPLAST MEMBRANE STRUCTURE SATORU MURAKAMI and LESTER PACKER From the Department of Physiology-Anatomy, University of California, Berkeley, California 94720 Downloaded from http://rupress.org/jcb/article-pdf/47/2/332/1069424/332.pdf by guest on 29 September 2021 ABSTRACT Light changes the structure of chloroplasts . This effect was investigated by high resolution electron microscopy, photometric methods, and chemical modification . (a) A reversible contraction of chloroplast membrane occurs upon illumination, dark titration with H+, or increasing osmolarity . These gross structural changes arise from a flattening of the thylakoids, with a corresponding decrease in the spacing between membranes . Microdensitometry showed that illumination or dark addition of H+ resulted in a 13-23% decrease in mem- brane thickness. Osmotically contracted chloroplasts do not show this effect . (b) Rapid glutaraldehyde fixation during actual experiments revealed that transmission changes are closely correlated with the spacing changes and therefore reflect an osmotic mechanism, whereas the light scattering changes have kinetics most similar to changes in membrane thickness or conformation . (c) Kinetic analysis of light scattering and transmission changes with the changes in fluorescence of anilinonaphthalene sulfonic acid bound to membranes revealed that fluorescence preceded light scattering or transmission changes. (d) It is concluded that the temporal sequence of events following illumination probably are proto- nation, changes in the environment within the membrane, change in membrane thickness, change in internal osmolarity accompanying ion movements with consequent collapse and flattening of thylakoid, change in the gross morphology of the inner chloroplast membrane system, and change in the gross morphology of whole chloroplasts . INTRODUCTION Ample evidence has been brought forward in changes in chloroplast membranes is still undeter- recent years to demonstrate, both in vitro (1-9) mined . and in vivo (10-13), the conditions under which This investigation was undertaken to elucidate light-induced proton and ion transport across the the sequence of steps by which changes in hydrogen chloroplast membrane leads to reversible changes gradients alter the gross morphology of the chloro- in the volume and configuration of these organel- plast membrane system . Our preliminary investi- les. Dilley and Vernon (2), Deamer, Crofts, and gations (14) have revealed that changes in the Packer (4), and Crofts, Deamer, and Packer (5) thickness of the thylakoid membrane are caused have suggested that changes in distribution of by the action of light and accompany the estab- hydrogen ions generated by light reactions of lishment of hydrogen gradients . This contraction chloroplasts play a central role in controlling the of the membrane is distinct from the more com- morphological changes following illumination, monly recognized "flattening" of the chloroplasts . although the precise mechanism whereby changes In order to clarify the nature of these microstruc- in hydrogen ions bring about the morphological tural changes, we initiated the present studies 332 THE JOURNAL OF CELL BIOLOGY . VOLUME 47, 1970 • pages 332-351 using such techniques as high resolution elec- pH Studies tron microscopy, microdensitometry, light-scat- For pH studies, chloroplasts were suspended in tering and transmission measurements, and 100 mm NaCl solution at pH 7 .8 (adjusted with 0.05 chemical probes, i.e., hydrophobic-seeking fluo- N NaOH) and then titrated with 0 .05 N HCI. Changes rochrome (8-anilinonaphthalene-l-sulfonic acid in pH of the incubation were measured with a glass [ANS]) and a sulfhydryl-seeking probe (phen- electrode inserted into the cuvette and connected to a ylmercuric acetate [PMA]) . Radiometer pH meter 22, the output of which was continuously recorded. MATERIALS AND METHODS PMA Binding Preparation of Chloroplasts Chloroplasts (13-15 µg chlorophyll /nil) were Spinach (Spinacia oleracea) leaves were homogenized in 50 mm Tris-HCl buffer, pH 8.0, containing 175 incubated for 4 min in 7 .5 ml of 50 mm Tris-HCI, mm NaCl . The homogenate was filtered through pH 8.0, containing 175 mm NaCl, 15 µM PMS, four layers of cheesecloth and centrifuged for 2 min and 20 µM PMA in the dark, in the light, and in the at 500 g to remove debris . The supernatant was dark following 5 min illumination. Neutral glutaral- Downloaded from http://rupress.org/jcb/article-pdf/47/2/332/1069424/332.pdf by guest on 29 September 2021 decanted and centrifuged again at 1500 g for 4 min . dehyde (N2 scaled, Polyscience Inc., Warrington, The chloroplast fraction was then washed once in an Pa.) was added at a concentration of 0 .1 M, and isolation medium by centrifugation at 1500 g for after 10 min the suspension was removed from the 6 min, resuspended in a small amount of the same cuvette and centrifuged for 10 min at 20,000 g. medium, and stored in an ice bath in the dark until The amount of unreacted PMA in the supernatant used in experiments performed at 25'C . was then assayed by dithizone (6 µg per ml chloro- For the study of photoshrinkage, isolated chloro- form) according to the procedure described by plasts were incubated in either sodium chloride- Miller et al . (15) from readings at 620 nm, and PMA medium (50 mm Tris-HCI, pH 8 .0, 175 mm the amount of PMA taken up by the chloroplast NaCl, 15 AM phenazine methosulfate [PMS] and membranes was calculated by difference from con- 20 µM PMA) or sodium acetate (150 mm sodium trols. acetate, pH 6 .7, plus 15 µM PMS) in the dark and then illuminated by red light. For osmotic studies, ANS Fluorescence chloroplasts were incubated in the dark in either 0.05 or 0 .5 M sucrose solution containing 44 mm To avoid artifacts from actinic light, the difference NaCl and 12 .5 mM Tris-HCI, pH 7 .9. in ANS fluorescence between unfixed and fixed chloroplasts was taken as a measure of the light- 90° Light Scattering and induced structural change. Chloroplasts were treated for 10 min with 0 .1 M glutaraldehyde, and then Transmission Studies washed three times by centrifuging for 10 min at Experiments were carried out in a cuvette in a 20,000 g . Chloroplasts thus "fixed" do not exhibit Brice-Phoenix light-scattering photometer (Phoenix any light scattering and transmission responses Precision Instrument Co., Philadelphia, Pa.) con- upon illumination . The reaction mixture contained nected to a dual channel recorder (recti/riter, Texas chloroplasts, 100 µg ANS and 15 µM PMS in the Instruments, Inc ., Houston, Texas) . The reaction dark, the fluorescence level was adjusted to read mixture was continuously stirred by a small magnetic 100%. Then the reaction mixture was illuminated bar . Light-induced changes in 90 ° light scattering or titrated with HCI in the dark . For experiments and transmission were recorded simultaneously . in a sodium chloride-PMA medium, PMA (20 To prevent a concentration-dependent interference gm) was added before illumination . Identical pro- by multiscattering of light by pigmented particles, cedures were used with fixed chloroplasts. Fluo- the chlorophyll concentration was kept less than 15 rescence was detected between 455 and 578 nm at µg per ml incubation medium. Within this range the low angle (20 ° ) to the exciting beam (290-404 nm) responses are proportional to concentration . The to prevent artifacts from scattering samples . measuring light was filtered at 546 nm with an in- terference filter, and the intensity in the dark before Electron Microscopy illumination or acidification of the suspension was adjusted to read 100% on the chart paper . Chloro- After 0.1 M glutaraldehyde treatment in the cuvette, plasts were illuminated by red light (600-700 run, reaction mixtures were transferred to test tubes and 900 ft-c) from the side of the cuvette opposite to the fixation was continued for 1 hr under continuous light-scattering measurement . light or dark. Samples were then treated with 1 % SATORU MtTRAKAMI ANn LESTER PACKER Protonation and Chloroplast Membrane Structure 3 3 3 osmium tetroxide in 50 mm phosphate buffer, pH electron microscope negatives (X 20,000) by micro- 7.4, and then washed with this buffer, dehydrated beam on the double-beam Microdensitometer MK with ethanol, and embedded in Epon-Araldite IIIC (Joyce Loeble & Co., Inc ., Burlington, Mass.) mixture (16) as modified by Johnson and Porter and recorded on the chart paper at 50 times ex- (17) . Sections were observed in an EMU-3H (RCA) pansion . The size of the microbeam used was about or Elmiskop I (Siemens) electron microscope with- 50 p., which is small enough to resolve the thickness out poststaining by heavy metal compounds. and spacing of the membranes even when they become tightly packed, because (a) the width of Dimension of Membranes the grana on the electron microscope negative is 200-300 p. and (b) the interspace or clear zone Thickness and spacing of membranes were esti- between two adjacent membranes is more than 80 µ mated by two methods : (a) direct measurement on at 50 times expansion . Measurement of half-width enlarged photographs at a final magnification of of the peak was done by extrapolating the slope of 200,000 by using a magnifier equipped with micro- the tracing to the background level as shown in scale and (b) microdensitometry tracing of electron Figs . 6, 10, 12, and 15. microscope negatives . In order to obtain measure- ments closest to real dimensions, certain precautions RESULTS Downloaded from http://rupress.org/jcb/article-pdf/47/2/332/1069424/332.pdf by guest on 29 September 2021 were taken . The grana portion of the membrane system was selected for measurement, since the Kinetics of Light Scattering and grana membrane is extremely flat, and is stacked Transmission Changes with membranes at constant spacing. Under such circumstances, the orientation of the membrane Photometric methods permit evaluation of the with respect to the direction of electron beam can dynamic aspects of light-induced changes in .
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